Bulletin de la Société entomologique de France, 122 (2), 2017 : 173-178.
Dactylopius opuntiae (Cockerell, 1896), a new invasive pest of the cactus plants Opuntia ficus-indica in the South of Lebanon (Hemiptera, Coccoidea, Dactylopiidae)
by Zinette Moussa1, Dany Yammouni1 & Dany Azar2 1 Laboratory of Entomology − Lebanese Agricultural Research Institute, Fanar, Lebanon
Abstract. − The scale insect Dactylopius opuntiae (Cockerell, 1896) (Hemiptera, Dactylopiidae) was detected for the first time in southern Lebanon in 2012, in the region of Nabatieh, on the cactus plantsOpuntia ficus-indica (L.) Mill. (Cactaceae). The survey conducted in 2014 showed that this new introduced species is widespread in the South of the country and that the damages are very severe on Barbary figs, whose fruits constitute additional income sources for farmers of the region. However, in 2015, new infestations were observed in the region of Jezzine and Chouf, situated at 18 km from the first site of detection. The predator Cryptolaemus montrouzieri (Coleoptera, Coccinellidae) was found in association with the colonies of D. opuntiae, but its densities were too low to regulate the population of this new invasive pest. D. opuntiae represents a considerable threat to the production of Barbary figs in Lebanon. Résumé. − Dactylopius opuntiae (Cockerell, 1896), un nouveau ravageur invasif des figuiers de Barbarie,Opuntia ficus-indica, au Sud Liban (Hemiptera, Coccoidea, Dactylopiidae). La cochenille Dactylopius opuntiae (Cockerell, 1896) (Hemiptera, Dactylopiidae) a été signalée pour la première fois au sud du Liban en 2012 dans la région du Nabatieh sur Opuntia ficus-indica (L.) Mill. (Cactaceae). La surveillance effectuée en 2014 a montré que ce nouveau ravageur est largement répandu au sud du pays et que les dégâts sont très sévères sur les figuiers de Barbarie dont les fruits contribuent au revenu des agriculteurs de la région. Cependant une nouvelle infestation a été observée en 2015 dans les régions de Jezzine et du Chouf, situées à 18 km du premier site de détection. Le prédateur Cryptolaemus montrouzieri (Coleoptera, Coccinellidae) était observé en association avec les colonies de D. opuntiae mais son abondance était insuffisante pour pouvoir contrôler la population de cette espèce envahissante. La cochenille D. opuntiae représente une menace considérable pour la production des figues de Barbarie au Liban. Keywords. – Scale insects, cactus pests, Barbary fig. ______
Dactylopius Costa, 1835 (Hemiptera, Dactylopiidae) is a genus of scale insects with only eleven species (De Lotto, 1974; Perez-Guerra & Kosztarab, 1992; Ben-Dov & Marotta, 2001; Van Dam & May, 2012). They feed exclusively on cacti plants of the genus Opuntia (Cactaceae) (De Lotto, 1974; Perez-Guerra & Kosztarab, 1992; Claps & de Haro, 2001). All the species of Dactylopius have similar appearance: body of an adult female is dark red, oval in shape and covered with white waxy filaments. Nymphs and adult females live in aggregations on cladodes usually at the base of the spines and feed on the sap causing the death of their hosts. In this context, five species of Dactylopius have been used successfully as biological control agents to eradicate Opuntia species in countries where cacti are considered as weeds (Moran & Zimmermann, 1984; Singh, 2004). In 1863, D. ceylonicus (Green, 1896) was introduced in Sri Lanka to control O. vulgaris Mill. (Tyron, 1910); D. opuntiae (Cockerell, 1896) was released against O. stricta (Haw.) Haw. in Australia in 1921 (Dodd, 1936; Hosking et al., 1994) and against O. ficus-indica Mill. in South Africa in 1933 (Annecke & Moran, 1978; Chávez-Moreno et al., 2011), whereas D. austrinus (De Lotto, 1974) was released onto O. aurantiaca Lindl. in South Africa (Moran et al., 1982). On the opposite, the cochineal Dactylopius become a major pest 174 Moussa et al. – Une cochenille ravageuse des figuiers de Barbarie au Liban in the regions where cactus plants have an economic importance in the agriculture production and the rural development as additional income sources for the farmers. In 2012, Dactylopius sp. was detected for the first time in the region of Nabatieh in the south of Lebanon on the cactus plant Opuntia ficus-indica. The pathway for the introduction in the country is still unclear. The identification of the genus was done by the laboratory of entomo logy at the Lebanese Agriculture Research Institute (LARI). For two consecutive years, the insect continued to disperse to other regions, attacking more cactus plants. In 2014, a survey was conducted by the LARI and the faculty of Sciences at the Lebanese University to study the distribution area of this new invasive pest and to evaluate the level of infestation of the cactus in order to implement a national strategy to manage the problem and reduce the economic losses of Opuntia ficus-indica in Lebanon.
Method of survey The survey was conducted between August 20th and September 22nd, 2014. Since the insect is host-specific, 90 sites were visited over the country based on the geographic distribution of Opuntia ficus-indica in Lebanon. According to Chalak et al. (2012), this cactus is cultivated along the coastal and the mountainous areas from the south to the north of Lebanon within an altitude of up to 900 m. It is found dispersed on the littoral and inland zones on the border of olives groves and other orchards or in backyards as a boundary hedge. However, seven commercial plantations with a surface area between 1 and 3 ha have been established: one in Batroun (Hamat), two in Chouf (Mazraet el Nahr), two in Hasbaya (Hasbaya), one in Tyr (Deir Anoun) and one in Qaa (Chalak et al., 2012). Samples of adult female of Dactylopius were collected from each infected site and conserved separately in 70% ethanol for the identification. All the sites were geographically coordinated by using a Global Positioning System in order to develop a map of distribution of the new invasive pest and the level of infestation on O. ficus-indica. Inter- views with local people were also conducted to collect additional information. The sites were classified into four categories according to the percentage of the surface of Opuntia cladodes infected by Dactylopius as following: 1) no infection; 2) low infection with less than 25% of the pad surface infected; 3) medium infection with 25-50% of the pad surface infected; 4) high infection with more than 50% of the pad surface infected.
Results Specimens collected from all the infected areas were identified in the laboratory of entomo logy at LARI as Dactylopius opuntiae (Cockerell, 1896) according to De Lotto (1974) and Perez-Guerra & Kosztarab (1992). The adult female is oval in shape and measures 2.1-2.3 mm long and 1.4-1.7 mm wide; however the female is sub-globular on slide and measures between 2.0-3.1 mm long and 1.8-2.7 mm wide. D. opuntiae is reported in South Africa, Mauritius, Madagascar, United States of America, Sri Lanka, Reunion, Mexico, Brazil, Australia, Jamaica, India, Hawaiian Islands, Kenya, Pakistan (Ben-Dov & Miller, 2015). In the Mediterranean region, it is recorded only from France on ornamental cactus (Foldi, 2001), Israel on O. ficus-indica (Spodek et al., 2014), Morocco on O. ficus-indica (Bouharoud et al., 2016) and here we record it for the first time in Lebanon. The survey showed that 55 of 90 sites were infested by D. opuntiae (table I). The distribution area of this scale was limited to the south of Lebanon from the coastal area to an elevation of 1047 m of altitude at Kaitouli village in the Jezzine District (fig. 1). The highest level of population was concentrated in the southern border, causing significant damages leading to the Bulletin de la Société entomologique de France, 122 (2), 2017 : 173-178 175
Table I. – Distribution of Dactylopius opuntiae (Cockerell) and level of infection on Opuntia ficus-indica (L.) Mill. in Lebanon (* new infestation of D. opuntiae detected in 2015). Number of sites infested by District Number of sites Level of infection D. opuntiae Batroun 2 – – Jbeil 7 – – Keserwan 3 – – Metn 1 – – Chouf 9 1* Moderate Sidon 4 – – Jezzine 8 1* Moderate West Bekaa 1 – – Rachaya 2 – – Hasbaya 13 13 Low - Moderate Nabatieh 20 20 High Tyre 13 13 High Beint Jbeil 7 7 High Total 90 55 death of the whole plants. However, during summer 2015, infestation appeared in new sites in Jezzine and Chouf Districts. During the interviews with local people, some wrong practices were noticed, where some farmers cut the infected parts of the cactus and threw them away to get rid of the problem, while others used them as hedges for their lands. Few numbers of the predator Cryptolaemus montrouzieri Mulsant, 1850 (Coleoptera, Coccinellidae) were observed in many sites in association with the population of Dactylopius. Only one site of infected cactus with a high population of C. montrouzieri was detected at the village of Kfardounin located at the southern border of the country.
Discussion The cochineal Dactylopius opuntiae was introduced accidentally to Lebanon in 2012 in the region of Nabatieh and it is well established in the south of the country in different ecosystems ranging from 0 to 1000 m above sea level where the specific host Opuntia ficus-indica is growing. The fast spreading of the insects within a short period of time is the result of biotic and abiotic factors such as the ability of this species to reproduce by parthenogenesis (Flores- Hermendez et al., 2006), the absence of natural enemies, the tolerance to environment variation and the availability of source of nutrients. The high level of infestation and the rapid spread of the cochineal in the districts of Nabatieh, Hasbaya, Beint Jbeil and Tyre in the southern regions were done mechanically by the local farmers due to negligence and lack of scientific knowledge of the biology and behavior of the insect. The progressive transition in the levels of infestation from high to moderate, then to low, is oriented from the South to the North, indicating that the insect has disseminated naturally. According to Moran & Cobby (1979), only the first instars known as “crawlers” are mobile and they climb up to the top of the cladodes from where they disperse to other cacti plants by wind. The presence of the predator C. montrouzieri in small numbers cannot alone control the population of D. opuntiae due to the ability of the pest to reproduce by parthenogenesis. A national strategy for management of Dactylopius opuntiae should be implemented based on the map of the levels of infestation (fig. 1). 176 Moussa et al. – Une cochenille ravageuse des figuiers de Barbarie au Liban
Conclusion The impact of D. opuntiae on O. ficus-indica was obviously catastrophic in the South where all the plants were completely destroyed. This impact affected negatively the socio-economic level of the farmers who depend on Barbary fig production to increase their incomes. The lack
Fig. 1. – Map of distribution of Dactylopius opuntiae (Cockerell) in Lebanon and level of infestation on Opuntia ficus-indica (L.) Mill. for 2014 and 2015. Bulletin de la Société entomologique de France, 122 (2), 2017 : 173-178 177 of awareness among farmers was the primary cause of increasing the outbreak of D. opuntiae in southern Lebanon. The risk of introduction of this pest to new areas is very high. Indeed, this new invasive pest has become a big concern for the prickly pear production in Lebanon and an eradication program should be implemented.
Acknowledgements. – We thank Dr Danièle Matile-Ferrero (Muséum national d’Histoire naturelle, Paris) for confirming the identification of the species Dactylopius opuntiae, and the student Mouhamad Abdalla (Faculty of Agricultural Sciences, Lebanese University) for his collaboration in this survey. Thanks are also given to the reviewers for their useful comments.
References
Annecke D. & Moran V., 1978. – Critical reviews of biological pest control in South Africa. II. The prickly pear, Opuntia ficus-indica (L.) Miller. Journal of the Entomological Society of Southern Africa, 41 : 161-188. Ben-Dov Y. & Marotta S., 2001. – Taxonomy and family placement of Coccus bassi Targioni Tozzetti, 1867 (Hemiptera: Coccoidea). Phytoparasitica, 29 (2) : 169-170. Ben-Dov Y. & Miller D. R., 2015. – ScaleNet: Systematic database of the Scale Insects of the World in the Catalogue of the Life. http://www.gbif.org/species. Bouharroud R., Amarraque A. & Qessaoui R., 2016. – First report of the Opuntia cochineal scale Dactylopius opuntiae (Hemiptera: Dactylopiidae) in Morocco. Bulletin OEPP/EPPO Bulletin, 46 (2) : 308-310. Chalak L., Younes J., Rouphael S. & Hamadeh B., 2012. – Morphological Characterization of Prickly Pears (Opuntia ficus-indica (L.) Mill.) cultivated in Lebanon. International Journal of Science and Research, 3 (6) : 2541- 2553. Chávez-Moreno C., Tecante A., Casas A. C. L. & Claps L. E., 2011. – Distribution and habitat in Mexico of Dactylopius Costa (Hemiptera: Dactylopiidae) and their cacti hosts (Cactaceae: Opuntioideae). Neotropical Entomology, 11 : 62-71. Claps L. & De Haro M., 2001. – Coccoidea (Insect: Hemiptera) associated with Cactacea in Argentina. Journal of the Professional Association for the Cactus Development, 4 : 77-83. De Lotto G., 1974. – On the state and identity of the cochineal insects (Homoptera: Coccoidea: Dactylopiidae). Journal of Entomological Society of Southern Africa, 37 (1) : 167-193. Dodd A., 1936. – The control and eradication of prickly pear in Australia. Bulletin of Entomological Research, 27 : 3503-517. Foldi I., 2001. – Liste des cochenilles de France (Hemiptera, Coccoidea). Bulletin de la Société entomologique de France, 106 (3) : 303-308. Flores-Hernández A., Murillo-Amador B., Rueda-Puente E. O., Salazar-Torres J. C., García- Hernández J. L. & Troyo-Diéguez E., 2006. – Reproducción de cochinilla silvestre Dactylopius opuntiae (Homoptera: Dactylopiidae). Revista Mexicana de Biodiversidad, 77 : 97-102. Hosking J., Sullivan P. & Welsby S., 1994. – Biolological control of Opuntia stricta (Haw.) Haw. var. stricta using Dactylopius opuntiae (Cockerell) in an area of New South Wales, Australia, where Cactoblastis cactorum (Berg) is not a successful biological control agent. Agriculture, Ecosystem and Environment, 48 : 241-255. Moran V. & Cobby B., 1979. – On the life-histrory and fecundity of the cochineal insect, Dactylopius austrinus De Lotto (Hemiptera: Dactylopiidae) a biological control agent for the Cactus Opuntia aurantiaca. Bulletin of Entomology, 69 : 629-636. Moran V., Gunn B. & Walter G., 1982. – Wind dispersal and settling of first-instar crawlers of the cochineal insect Dactylopius austrinus (Homoptera: Coccoidea: Dactylopiidae). Ecological Entomology, 7 (4) : 409-419. Moran V. & Zimmermann H., 1984. – The Biological control of cactus weed: achivements and prospects. Biocontrol News and Information, 5 : 297-320. 178 Moussa et al. – Une cochenille ravageuse des figuiers de Barbarie au Liban
Perez-Guerra G. & Kosztarab M., 1992. – Biosystematics of the family Dactylopiidae (Homoptera: Coccinea) with emphasis on the life cycle of Dactylopius coccus Costa. Studies on the morphology and systematics of scale insects. Bulletin of the Virginia Agricultural Experiment Station, 92 (1) : 1-90. Singh S., 2004. – Some success stories in classical biological control of agricultural pest in India. Bangkok : Asia-Pacific Association of Agriculture Research Institutions (APAARI), FAO Regional Office for Asia and the Pacific, iv + 52 p. + appendix. Spodek M., Ben-Dov Y. P. A., Carvalho C. & Mendel Z., 2014. – First record of Dactylopius opuntiae (Cockerell) (Hemiptera: Coccoidea: Dactylopiidae) from Israel. Phytoparasitica, 42 (3) : 377-379. Tyron H., 1910. – The wild cochineal insect, with reference to its injurious action on prickly pear (Opuntia spp.) in India etc., and to its availability for the subjugation of this plant in Queensland and else- where. Queensland Agricultural Journal, 25 : 188-197. Van Dam A. & May B., 2012. – A new species of Dactylopius Costa (Dactylopius gracilipilus sp. nov.) (Hemiptera: Coccoidea: Dactylopiidae) from the Chihuahuan Desert, Texas, U.S.A. Zootaxa, 3573 : 33-39. ______